Levels of selection and the evolution of social organization

This dissertation investigates the role of genetic elements that are involved in evolutionary conflicts across multiple levels of biological organization in the evolution of social organization and other complex biological phenomena. Specifically, it explores the role of the Gp-9b element in the evolution and maintenance of social organization in the fire ant Solenopsis invicta. The Gp-9b element appears to be engaged in evolutionary conflicts at three levels: (1) at the level of intragenomic conflict the Gp-9b allele biases genetic transmission in its favor by mediating the execution, in colonies where it is present, of female sexual offspring that do not bear the allele. (2) At the level of selection among individuals the Gp-9b allele imposes physiological effects on its bearers, including reproductive inviability in homozygotes and reduced dispersal ability in heterozygotes, that appear to entail significant selective costs. (3) At the colony level the Gp-9b allele confers the polygyne social phenotype which appears to have numerous ecological advantages in direct competition with the mongyne form in which all individuals possess the alternate Gp-9B allele.; A conceptual model is presented describing evolutionary processes by which selfish genetic-drive elements, favored by natural selection operating at levels below the individual organism, can impose constraints on individual reproduction that render cooperative strategies attractive to their carriers. Such selfish elements often create balanced polymorphisms and thus lend themselves to the evolution of complex linkage groups. Subsequently, positive higher-level selection can facilitate the elaboration of such coadapted gene complexes beyond the point at which their expansion would otherwise be constrained by deleterious effects on individual fitness. This process can lead to the evolution of still greater constraints on independent reproduction.; The S. invicta Gp-9 system is examined in detail with respect to the role of Gp-9 in the evolution of social organization. The Gp 9b allele remains at high frequencies in wild populations despite acting as a recessive lethal. A second seemingly parodoxical feature of the social biology of introduced S. invicta is that reproductive nestmate queens in polygyne S. invicta nests are unrelated. A mechanism is described by which a selfish genetic element linked to Gp-9b may spread within populations, despite deleterious effects on individual queens, by promoting polygyne social strategies that are successful in competition with the monogyne (single queen per colony) form at the level of selection between colonies. The interaction between the Gp-9b allele and social organization appears to create a selective regime that promotes divergence between the two social forms by making polygyne social strategies obligate to carriers of the allele and by favoring the evolution of a large selfish linkage group comprising numerous alleles that specify diverse aspects of the polygyne social phenotype.; Empirical evidence is presented regarding the relationship between Gp-9 genotype, social organization, and queen reproductive phenotype in native South American populations of S. invicta. The two alleles at this locus present in introduced populations, B and b are shown to have effects on queen phenotype that are similar to those exhibited in the introduced range. A third allele, b*, that exhibits close sequence similarity to allele b and, like b, is restricted to the polygyne social form, also appears to have effects similar to b's on queen phenotype. Significantly, the two polygyne alleles do not coexist in individual colonies, suggesting the operation of some social or ecological segregating mechanism. These results provide significant support for the idea that constraints on independent reproduction, associated with Gp-9 genotype, have played an important role in the evolution and persistence of polygyny in S. invicta.